Biological Control and Invasive Species Management in the United

S
ince 1993, graduate students in entomology
or a related discipline have organized and participated in a debate hosted at the national
meeting of the Entomological Society of America.
Topics selected are generally of current interest to
the students, as well as to the entomology community and the public. Huberty (2003) provides a
summary of the debate guidelines, which traditionally have
b e e n
very
lowed by pro and con summaries. Because of space
constraints, each team was allowed 500 words to
summarize their position in publication. Consequently, some positions may be more thoroughly
developed than others.
TOPIC
Classical Biological Control of Exotic Insect
Pests Involves Unacceptable Ecological
Risk to Native Insect Species
Introduction
Fred Gould
Department of Entomology, North Carolina
State University
Since the 1930s, there have been numerous textbook examples of biological control efforts gone amok. The
extinction of more than six reptile
species due to the introduction of
the mongoose for biological control and the havoc wrought by
the cane toad in Australia are
often cited.
Historically, the major
nontarget problems caused
by classical biological control
of insect pests were associated with vertebrates.
Entomologists often pointed
to the differences between
insects and vertebrates as a
reason for less concern with
insect biological control
agents. Furthermore, entomologists also cited improvements in prerelease screening
tests that checked for the host
range of biological control agents.
In 1983 and again in 1991, F. G.
Howarth called on entomologists to
reexamine the potential for nontarget
effects that could result from release of
insects as biological control agents.
Howarth was especially concerned about the
potential of exotic herbivores, predators, and
parasites to attack endemic or endangered species.
He presented several cases in which there was some
evidence that insect species used for biological control had caused damage to nontarget species.
Since Howarth challenged what he believed was
complacency on the part of entomologists, a cadre
of entomologists, ecologists, and conservationists
have begun to conduct more detailed experimental
analyses of the hypothesis that biological control
agents do not cause environmental damage. Biological control practitioners also have increased
efforts at testing the host range of species being
considered for use. Furthermore, federal regulatory practices related to introduced biological
control agents are being reassessed.
and Invasive
Species Management
in the United States:
A Student Debate
Jeffery K. Tomberlin
structured.
The topics
and the position of
argument (pro vs. con) were
randomly assigned to the debate teams.
Four questions regarding biological control and
invasive species in the United States were selected
as topics for the debate held at the 2000 joint meeting of the Entomological Society of America, the
Entomological Society of Canada, and the Societe
d’Entomologie du Québec, Montreal, Canada. For
each topic, there is a nonbiased introduction, fol238
AMERICAN ENTOMOLOGIST • Winter 2003
Beyond scientific inquiry and assessments, the
debate about the potential negative effects of biological control has moved into the public arena.
Many practitioners of biological control who consider themselves to be environmentalists have been
astonished by the public criticism leveled against
them by other environmentalists. After decades of
their “labor of love” to replace the use of broadspectrum pesticides with natural control agents,
many biological control practitioners believe that
their accusers are misdirected or disingenuous.
Some of the public critics believe that biological
control is the most powerful under-regulated environmental technology in the United States, and
that, for defensible or indefensible reasons, the
practitioners have been ignoring a critical issue. Of
course, many biological control practitioners and
environmentalists do not hold such polarized views.
In preparation for this debate, the students have
been examining the information on nontarget
effects for a few months. Notice that the focus of
this debate between the University of Maryland
and the University of California at Davis is limited
to ecological risks associated with biological control of exotic insect pests and not with the control
of weeds. The debate also focuses on classical biological control as contrasted with augmentative releases or practices that enhance the conservation
of biological control species in managed systems. It
was our hope that the audience, and perhaps even
the debaters themselves, would leave the forum with
a deeper understanding of the issues involved.
Pro Position
Scott M. Ferrenberg, Ethan C. Kane, Andrew H.
Smith, and Mark E. Suarez
University of Maryland
Given the growing potential for introductions of
invasive species, comprehensive management strategies must be devised. Some advocate classical
biocontrol as the best alternative for combating
invasive species. Although biological control has
been effective in certain situations, it is our position that this approach poses unacceptable risk to
native insects.
The characteristics that make insects ideal models for evolution and genetic studies, including high
fecundity, short generation times, and high dispersal ability, should also raise concern when contemplating their release as biological control agents.
Successfully introduced agents typically are permanent additions to the environment, and as such,
they may cause irreversible, negative effects (Elliott
et al. 1996).
Sufficient examples of nontarget effects exist,
warranting concern (Simberloff and Stiling 1997).
Strong (1997) notes that 32% of the 115 parasitoids introduced into Hawaii attack native insects
other than their intended targets. Similarly,
Hawkins and Marino (1997) report that 16% of
parasitoids introduced into North America have
colonized native hosts. Additionally, the tachinid
fly, Bessa remota (Aldrich), which was introduced
AMERICAN ENTOMOLOGIST • Volume 49 Number 4
into Fiji, parasitizes only nontarget organisms
(Howarth 2000).
Another example, involving a European tachinid
fly, Compsilura concinnata (Meigen), which is used
to control gypsy and browntail moths [Lymantria
dispar (L.) and Euproctis chrysorrhoea (L.)] in
North America, also demonstrates nontarget
effects. Lacking synchronization with its target
pests, this agent attacks nontargets during three of
its four generations in a year (Howarth 2000). Studies link this tachinid to the decline in giant silk
moths, Rothschildia jacobaeae Walker, in northeastern North America (Howarth 2000). There is
also evidence that Coccinella novemnotata Herbst,
a native coccinellid, has declined as a result of the
introduction of Coccinella septempunctata L. (Elliot
et al. 1996).
Biological control advocates state that nontarget effects are minor, but little effort has been
directed at measuring the long-term impacts of such
events (Strong 1997). Howarth (1983, 1985,
1991) has argued that biological control introductions have likely caused extinctions of nontarget
organisms. Limited knowledge about arthropod
assemblages prior to introductions of control agents
limits our ability to assess nontarget effects and
extinctions.
Not only can classical biological control result
in trophic alterations, but the overwhelming percentage of classical biological control attempts have
failed to achieve an economically effective level of
pest control. From 1880 to 1998, there were more
than 4,500 classical biological control attempts,
and only about 10% of these led to some level of
pest management (Gurr and Wratten 2000). Given
the high stakes of invasive species scenarios, a
control methodology as unreliable and as risky as
classical biological control is not our best primary
option.
Not only can classical
biological control
result in trophic
alterations, but the
overwhelming
percentage of classical
biological control
attempts have failed
to achieve an
economically effective
level of pest control.
Con Position
David R. Haviland, Kirsten A. Copren, Cheryle A.
O’Donnell, and Tamara L. Roush
University of California, Davis
Classical biological control is one of the most
under-appreciated and under-valued control
tactics available for the management of exotic
insect pests. The potential specificity, permanence,
and affordability that this tactic offers make it a
primary candidate in any integrated pest management (IPM) strategy. When executed properly,
economic control can be exerted on extremely
injurious exotic pests with minimal risks to native
insect species.
Pressures from exotic pests constantly influence
agricultural and urban environments. Pimentel et
al. (1999) estimated that 4,500 arthropod species
have been introduced into the United States. This
report predominantly includes accidental introductions that were unscreened, not researched, and
often imported unknowingly by people ignorant
of ecological and environmental issues. Many of
these introductions represent enormous risks to
239
native insect species, risks that justify consideration
of classical biological control.
Risks associated with the importation of
natural enemies can be
minimized through
appropriate
preintroduction
assessment proGiven the right conditions,
cesses. These
with the proper control
procedures
weed out
agent, there is no other
candidate
tactic that can equal the
organisms
that poseffectiveness of classical
sess the
biological control. This tactic
potential to
shift hosts,
is unparalleled for its ability
expand beto permanently correct
yond desired
geographical
invasive pest problems
ranges, or negawithout insecticide use.
tively
affect
endemic or endangered insects. These
processes also separate
the modern era of biological
control from the often-criticized early period of ad
hoc introductions. Currently, to properly assess
risks, researchers must possess, at minimum,
knowledge about the biology of the control agent,
including host range and specificity. Decisions are
made only after all available options, such as
cultural and native biological control, are considered.
The risks of not implementing classical biological control should also be considered. This is particularly true with the use of default insecticide
applications. Risks from insecticides on native
insect species far outweigh the risks of biological
control, especially with properly screened introduced organisms. Imagine the worldwide citrus
industry without the vedalia beetle, Rodolia
cardinalis (Mulsant), to control cottony cushion
scale, Icerya purchasi Maskell. Industry survival
would have required an arsenal of insecticides. Similarly, without the introduction of Encarsia inaron
(Walker) for ash whitefly, Siphoninus phillyreae
(Haliday), management, recreation areas and
urban landscapes in many U.S. cities would still be
applying insecticides repeatedly.
Given the right conditions, with the proper control agent, there is no other tactic that can equal the
effectiveness of classical biological control. This tactic
is unparalleled for its ability to permanently correct
invasive pest problems without insecticide use, as well
as its capacity to do so in a manner that is efficient,
economic, and safe to native insect species.
Acknowledgment
We thank Les Ehler and Michael Parrella for
their helpful comments in the preparation of our
statement. Also, we thank the University of California, Davis, Department of Entomology for funding our attendance at the debate.
240
TOPIC
Classical Biological Control of Exotic Weed
Species Involves Unacceptable Risk to
Native Plant Species
Introduction
Will K. Reeves
Clemson University
Since the invention of agriculture and agricultural
trade, exotic plants have been introduced into nonnative habitats by human activities. Most exotic
plants do not survive, but some become “weeds”
after introduction. These weeds are rather broadly
defined as any noxious, unsightly, or unwanted
plant. Some weeds are endemic species, but up to
75% of the problem weeds in the United States are
considered exotic plants (Delfosse 1988).
Mechanical and cultural agricultural practices
or herbicides have dominated the traditional methods of weed control. Biological control is another
option, which is most often considered for weed
control when pest plants are not localized or traditional methods give inadequate results. Most biological control programs are conducted on extensive, low-value lands (i.e., range lands) where traditional control practices are prohibitively expensive.
In addition to saving money, the public often
perceives biological control as an environmentally
friendly alternative to chemical control (Louda et
al. 1997). Government agencies that favor chemical reduction also support biological control
(Malakoff 1999).
Biological control is a component of most IPM
strategies. By definition, IPM does not rely on a
single control method to reduce pest species below
an acceptable damage level. In classical biological
control strategies, self-reproducing populations of
herbivores are established to control target weeds.
These herbivores reproduce and redistribute themselves into new weed populations. Chemical
control practices are usually reduced or eliminated.
Classical biological control using herbivorous
insects has been successful in reducing weed populations (e.g., Klamath weed) (Crawley 1989); however, the eventual fates of exotic herbivorous
species are hard to predict. By definition, a successful classical biological control program must leave
viable exotic herbivores and weeds in the ecosystem. The ecological effects of these introduced herbivores cannot be fully determined before release.
For example, the flowerhead weevil, Rhinocyllus
conicus Froeh, was released to control the Russian
thistles and now is attacking other native and
exotic thistles (Louda et al. 1997, Strong 1997).
Numerous other examples exist of introduced
biological control agents attacking nontarget
native plants or feeding on unexpected food sources
(Howarth 1991). The risks of introducing populations of exotic herbivores must be considered
against the environmental and economic costs of
targeted weed species. Biological control is a “hitAMERICAN ENTOMOLOGIST • Winter 2003
or-miss” method of pest control, and less than one- nently in a new environment (Ehler 1991). Somethird of the introduced herbivorous species have times this is accomplished because selection
become established in the United States (Malakoff pressures are removed when the agent is taken from
1999). Only 20–40% of all biological control strat- its native habitat (Dethier 1952). Chrysolina
egies for exotic weeds have been successful (Louda quadrigemina (Suffrain) was successfully released
et al. 1997). Still, successful biological control can in California and provided good control of
be more effective than herbicides and costs less to Klamath weed, Hypericum perforatum L., by 1956
maintain. If exotic herbivores are prolific and host- (van den Bosch and Messenger 1973). When this
specific, the benefits of biological control agents insect was found damaging the ornamental H.
can exceed the effectiveness of other control meth- calcynum L. in 1976, it was attributed to evolution
ods.
of a host race (Andrés 1985). Harris (1990) proCritics of classical biological control often refer posed that selection for host strains may occur
to the apparent lack of regard for the environment when the agent experiences improved survival on a
when biological control species are released marginal host, for example, Teleonomia scrupulosa
(Howarth 1991, Strong 1997). Their opponents Stål temporarily attacking sesame, Sesamun
counter by arguing that stringent host specificity indicum L., after defoliating lantana, Lantana
tests as well as ecological and economic evalua- camara L.
tions are undertaken before release (McEvoy 1996,
One desirable attribute of an effective natural
Malakoff 1999). Evidence indicates that some enemy is the ability to disperse; however, the inabilintroduced weed-controlling species have caused ity to restrict dispersal of a permanent agent places
ecological disasters (Howarth 1991). Even some native plants at risk. Cactoblastis cactorum
highly successful biological control campaigns have Bergman was released in 1957 in the Leeward
suffered negative publicity when control agents Islands to control Opuntia spp. (van den Bosch
escaped laboratories before their intended
and Messenger 1973). In 1989, this moth
release (Finkel 1999). The ecologiwas observed in the Florida Keys
cal damage caused by failed
feeding on the endangered
biological control agents must
Opuntia
spinosissima
be considered when any
(Martyn). This example
new agent is proposed.
demonstrates that even if
Biological control will
thorough prerelease
Factors that place native
remain a component of
studies are conducted,
plant species at risk
IPM. Like most pest
predicting negative efinclude genetic change,
management practices,
fects from unforeseen
there are no simple
dispersal of the biodispersal of the weed
solutions that lack pitlogical control agent to
control agents, and
falls. All complications
new areas is difficult
must be considered
and
risky.
greatly limited
carefully before new
No absolute tests unprerelease studies.
biological control agents
equivocally anticipate the
are released. Strict laboraoutcome of inserting a
tory and field tests must be
novel species into an ecosysdone to determine the ecologitem or likewise determine
cal risks involved with introduced
whether native plant species will
biological control species. If herbivobe affected by the release of biological
rous species are not an environmental risk, then control agents (Zwolfer and Harris 1971). Tests
the costs and benefits of their use as a biological are carried out in artificial environments (i.e., cages,
petri dishes); therefore, the ability to accurately
control agent must be considered.
predict weed control agent behavior in the target
habitat is difficult. Prerelease studies are being
Pro Position
Melissa M. Willrich, Boris Castro, and Jeff Gore expanded for phylogenetic testing; however, negative (nontarget) effects on the plant ecosystem may
Louisiana State University
not be readily evident for 20–30 years.
In a recent survey, biological control experts
Biological weed control is often considered to be a
safe and effective way to provide permanent were asked to identify issues of most concern and
control with little or no damage to nontarget the challenges they face in implementing classical
organisms and no ecological disruptions (van den biological control programs. Of the 115 surveyed,
Bosch and Messenger 1973, DeBach 1974). How- 80% indicated as the issues of most concern: (1)
ever, numerous examples exist of biological weed inability to predict nontarget negative impacts and
control agents damaging nontarget plants. Factors (2) lack of post-release evaluations (Marshall W.
that place native plant species at risk include ge- Johnson, University of California at Riverside,
netic change, dispersal of the weed control agents, unpublished data, 1995). In conclusion, it is
estimated that less than 40% of introduced agents
and greatly limited prerelease studies.
Biological control agents must adapt (geneti- against weeds and insects result in substantial
cally) to become established and persist perma- control (Thomas and Willis 1998). Our position is
AMERICAN ENTOMOLOGIST • Volume 49 Number 4
241
that this level of possible success is not high enough
to justify the potential long-term risk to nontarget
plants associated with introducing biological weed
control agents.
Acknowledgment
The authors thank Gene Reagan and Seth
Johnson for their help and guidance in preparing
our argument and this manuscript.
Con Position
David W. Held, Jerome A. Gels, Eric J. Marsland,
and Marissa L. Griffin
University of Kentucky
Exotic weeds can completely impact all biotic and
abiotic components of native ecosystems, greatly
diminishing the abundance and survival of native
species (Mack et al. 2000). Failure to control invasive weeds can result in severe global consequences,
including loss of agricultural, forestry, and fishing
resources (Mack et al. 2000). The environmental
consequences of allowing exotic plants to proliferate are profound, and the benefits associated with
the judicious selection of a classical biological agent
far outweigh any risks.
Classical biological control of invasive weeds
uses exotic herbivores from the same habitat as the
problem weed. In the United States, successful use
of classical biocontrol agents for weeds range from
41% exerting some control to 20% yielding
significant control (Harris 1993, Louda et al. 1997).
Significant control of rampant exotic weeds is
difficult to achieve through other conventional
means. Compared with other methods, the minimal nontarget effects and low input solutions
achieved by successful classical biological control
make it an environmentally and economically sound
alternative.
A cautious selection process reduces the environmental risk associated with importing an
exotic herbivore to control an alien weed (Harris
1993). Although host switching by a control agent
is the predominant concern associated with classical weed biological control, 600 examples throughout the world show that control agents
have remained within their
predicted host range (Harris
1993). Furthermore, there
are only eight recorded
instances in which biological control agents
Success, economics,
have attacked plants
and sustainability
other than their
initial
targets
suggest that classical
(McFayden 1998).
biological control
Of these, five were
remains the best option
known to attack
native plants within
for the control
the same genus of the
of exotic weeds.
target plant. At the time
of introduction, however, the other plants were
not considered to be eco242
nomically important. By today’s screening criteria,
these insects would have been eliminated as candidates for use, and these problems would not have
occurred (McFayden 1998).
Eliminating exotic insect herbivores as potential control agents for invasive weeds is not an
option. The successful control of alligator weed,
Alternanthera philoxeroides L., and klamath weed,
Hypericum perforatum L., through classical biological control illustrates the failures associated with
cultural and chemical control, reiterating why classical biological control is such an important tool.
The extensive and remote coverage of these weeds
rendered cultural control too expensive and futile
(Harley and Kassultke 1971, Julien and Chan
1992). Herbicides used to treat alligator weed were
not only ineffective and costly, but also reduced
nontarget native flora (Julien and Chan 1992).
Simultaneously, Alligator weed was becoming resistant to herbicides and thus out-competed native
plants (Julien and Chan 1992). Other methods,
which use native herbivores to control exotic weeds,
have been unsuccessful (Harris 1993, McFayden
1998). Success, economics, and sustainability
suggest that classical biological control remains the
best option for the control of exotic weeds.
TOPIC
Local Communities Should be Able to Block
Efforts to Control Invasive Exotic Species
within Their Boundaries, if They Consider the
Methods to be Used Unacceptable
Introduction
Boris Castro and Jeff Gore
Louisiana State University
Many insects, weeds, and plant pathogens have
been either purposely or accidentally introduced
into the United States (Horsfall 1983). Upon
arrival, some of these organisms have become
established and caused economic or ecological
damage. Pimentel et al. (2000) estimate that exotic
species are responsible for more than $138 billion
in losses and control costs annually. Invading
species that become established often proliferate
rapidly and become devastating pests (Horsfall
1983, Mack et al. 2000). Mack et al. (2000) attributed success of exotic species to three factors. These
include (1) loss of biological constraints, (2)
utilization of a vacant niche, and (3) lack of community species richness.
Control of exotic species is an often difficult
and controversial subject. Several methods have
been used to manage exotic species in the United
States, and citizens have opposed some of these
methods. Perhaps the most publicized method for
controlling exotic species has been eradication
efforts. Eradication efforts have been very effective
in some instances and disastrous in others. The
eradication of the screwworm fly, Cochliomyia
hominivorax (F.), is one of the most successful
AMERICAN ENTOMOLOGIST • Winter 2003
examples of an eradication effort (Simberloff 1997).
The sterile male release technique used in this program has been adopted for other eradication efforts because of its widespread success. Sterile males
of the Mediterranean fruit fly, Ceratitis capitata
(Wiedemann), were released for eradication in
California, but reinfestations of the Mediterranean
fruit fly in the state caused this program to be far
less successful than the screwworm project. Applications of malathion were made to help eradicate
the Mediterranean fruit fly, despite opposition from
the public (Kahn et al. 1990).
In 1957, Congress authorized $2.4 million dollars to begin eradication of the red imported fire
ant, Solenopsis invicta Buren (Lofgren 1986).
Initial eradication efforts used widespread applications of heptachlor, an insecticide that is very toxic
to nontarget organisms, including humans. Wildlife and cattle died as a result of the initial applications (Davidson and Stone 1989). Florida and other
states withheld matching funds, and heptachlor
applications were discontinued. Eradication
attempts against the red imported fire ant were
continued with the development of mirex bait.
Mirex residues, however, were found in many nontarget organisms; and the U.S. Environmental Protection Agency canceled mirex’s registration in 1977
(Lofgren 1986). The cost of these eradication efforts was approximately $200 million; and the fire
ants’ range actually expanded during the time of
treatment (Davidson and Stone 1989). The range
expansion was primarily due to mirex adversely
affecting native ant species, thereby reducing competition with red imported fire ants.
Other control methods include maintenance
control (Schardt 1986), ecological restoration
(Randall et al. 1986), and biological control (Center et al. 1986). Maintenance control has been very
effective against exotic weed species. In Florida,
multiple chemical and mechanical control tactics
are used to maintain water hyacinth, Eichhornia
crassipes Solms, and hydrilla, Hydrilla verticillata
Royle, below damaging levels (Schardt 1986). These
kinds of programs have been successful and experienced little public opposition.
Ecological restoration is perhaps the most complete and ecologically sound method for reducing
effects of exotic species. This kind of control is
used primarily in natural areas following disturbances that are not likely to be reversed without
intervention (Cairns 1986). The ultimate goal of
this kind of program is to allow native species to
replace exotic species (Randall et al. 1986). One
example of this involves suppression of wildfires.
In areas where wildfires are common, the organisms in that habitat are adapted to (and often benefited by) fire. Consequently, when wildfires are
suppressed, exotic species can invade the habitat,
leading to changes in the ecosystem. If wildfires are
encouraged in these habitats, invading species will
usually be reduced (Ewel 1986).
Another example involves mine reclamation.
Mining sites have been heavily disturbed and are
very susceptible to invasion by exotic species. The
AMERICAN ENTOMOLOGIST • Volume 49 Number 4
result of mine reclamation projects may be ecological restoration or replacement with a new habitat
(Randall et al. 1986).
Classical biological control is based on the
premise that an exotic species’ population is not
regulated by biological constraints that are present
in its native habitat. With classical biological control, the native habitat of the exotic species is
explored for natural enemies, which are then imported and released into the new habitat (DeBach
1974). Classical biological control has been used
successfully against insects, plant pathogens, and
weed pests. The most successful and well-known
case of classical biological control involved importation of the vedalia beetle, from Australia to control the cottony cushion scale in California citrus
(Caltagirone and Doutt 1989). This method is very
logical; however, some oppose the importation of
another exotic species, fearing unknown effects.
All of the control measures mentioned here have
benefits and risks. Among these measures,
eradication is the most controversial
method for controlling exotic pests.
These programs can be very expensive, and in general, the probabilThe most successful and
ity of success is small. However,
well-known case of
certain organisms are good candidates for eradication. This
classical biological control
was particularly true of the
involved importation of
screwworm fly. Information
about the biology and mating
the vedalia beetle, from
habits of this pest was essential
Australia to control the
to the success of the program. In
cottony cushion scale in
contrast, methods used in red imported fire ant eradication were inCalifornia citrus
appropriate and not well studied; and
disastrous effects could have occurred.
In conclusion, any method used to control an exotic species is likely to be criticized by
some individuals. Different people will have different views as to the importance of controlling pests.
In general, public perceptions of risks associated
with a control measure (or an exotic species) will
likely be different than the risks perceived by scientists and researchers (Higley et al. 1992). The Biological Control Act of 1984 (Anonymous 1984)
was enacted in Australia in response to conflicting
interests about biological control of the weed
Echium plantagineum L. This act allows for public
review of biological weed control programs before
release of the biological control agent (Goeden and
Andrés 1999). Certainly, local communities should
be able to voice their concerns about control measures within their borders; however, allowing local
communities to block control efforts is a much
deeper concern that should be closely evaluated.
Pro Position
Michelle G. Colacicco, R. Chitkowski, and Austin
Jenkins
Department of Entomology, Clemson University
Communities should have the right to reject or
limit eradication and control programs because
243
mandatory participation in pest management programs can adversely affect local areas. Taking away
the rights of the local constituency to evaluate the
programs that are enacted within their boundaries
degrades the integrity of the community. Local areas must be empowered to evaluate proposed pest
management programs and alter them to meet the
needs of their citizens. Ultimately, if the majority of
community members deem a proposed program
unacceptable, they should be able to block control
programs within their boundaries.
Health problems and monetary losses often
result from eradication programs. For example,
the medfly eradication programs in California and
Florida led to apprehension and mistrust in local
communities (Kahn et al. 1990). Residents exposed
to pesticide sprays suffered from respiratory, gastrointestinal, dermatological, and neurological
disorders (Shafey et al. 1999). In
addition to these health
problems, some pesticide applications
damaged private
To be effective, any
property;
In
C
a
l
i
f
o
r
n
i
a
,
management effort should fall
14,000 claims
within a centrally managed
for automobile paint
framework where
damage cost
coordination, regulation,
the state taxpayers $3.7
and accountability
million (Myers
maximize the probability
et al. 1998).
Community
of effective control.
members should
have the opportunity
to evaluate proposed
management programs for
potential negative impacts. If the impacts or risks of a proposed eradication program
outweigh the benefits, community rights should
prevail and must be considered by planners.
Management of invasive species can include
cultural and habitat modifications. The implementation of these programs has the potential to economically injure local industries and communities.
For example, the boll weevil eradication program
forced farmers to alter their farming practices by
requiring them to participate in timed spraying,
habitat destruction, and trap cropping (Myers et
al. 1998). All of these control measures required
time and money that could have been used to maintain farms. Local communities should be able to
evaluate and, if necessary, veto programs that
require unacceptable cultural modification, monetary loss, or habitat destruction.
Some individuals, industries, and communities
can benefit from exotic species that are considered
pests by others. Because most exotic pests cannot
be totally eradicated, a universally enforced eradication or control program can affect communities
that benefit from exotic species. Exotic “pests” have
been beneficial in certain situations. Data has accumulated suggesting that the red imported fire ant
244
can be a valuable beneficial in some agricultural
systems and to pest control operators. (Vinson
1997, Meyers et al. 1998, McGriff and Ruberson
1999). Communities should be able to determine
whether a targeted species is a pest to their citizens.
In summary, community opinions and rights
must be considered during all stages of a control
program. When a community will be harmed from
a program, it should have the right to refuse to
participate.
Con Position
Patrick S. Duetting, Mary M. Gardiner, Addie R.
Polerstock, and April A. Stehr
Department of Plants, Soils, and Entomological
Sciences, University of Idaho
Exotic invasive species cause serious economic,
biological, health, and social problems. After habitat destruction, non-native species are the second
largest threat to biodiversity (Devine 1999). In the
absence of natural enemies, exotic species gain a
competitive advantage over native species. This may
result in an irreversible impact on ecosystem function; therefore, control demands a plan based in
sound biology.
Local communities should not be able to block
efforts to control invasive exotic species because
complete implementation of an area-wide management plan executed along biological boundaries is
essential. If the invasive species is not managed
throughout the invaded region, control efforts will
fail because of pest refuges in unmanaged areas. Individuals remaining in these refuges can comprise
metapopulations—populations that are linked by
dispersal (Husband and Barrett 1996, Gillman and
Hails 1997). Re-establishment subsequent to local
extinction is possible because of the potential for
dispersal of local breeding populations (Hanski and
Simberloff 1997). Movement from unmanaged
areas allows recolonization and spread. If a local
region within the target area is not included, the
entire control program will not be effective.
Furthermore, plans developed for release and
management of biological control agents are based
on modern scientific theory and research and are
in accordance with EPA and USDA guidelines (U.S.
Congress, OTA 1993). Communities have the opportunity to be involved in the development of these
plans. An appropriate framework exists for determining whether control tactics pose acceptable risks.
To be effective, any management effort should
fall within a centrally managed framework where
coordination, regulation, and accountability maximize the probability of effective control. Without
oversight, exotic invasive species can expand in
range outside the political boundaries of a local
control program. Instead of leaving control of exotic invasive species to local communities, interagency cooperation, public education, and public
involvement should be encouraged.
Control of invasive species should operate under a strong body of law. Exotic invasive species
should be considered pollutants comparable with
AMERICAN ENTOMOLOGIST • Winter 2003
oil spills, hazardous waste discharges, or other
events that damage public environmental resources.
Control of these species is done for the good of the
people and should not be blocked by local interests. The maintenance of the health and quality of
ecosystems and the preservation of biodiversity are
within the public domain and should be acknowledged as a public right.
Acknowledgments
We thank Nilsa Bosque-Perez and Mark
Schwarzlaender for their time, guidance, and
support throughout the preparation of this
debate. We thank Sanford Eigenbrode, Joseph
McCaffrey, Frank Merickel, and Jack Brown for
their comments and input.
TOPIC
Because Increasingly Open Trade Increases
the Risk that Invasive Exotic Species will be
Introduced into the United States, an
Environmental Impact Assessment (EIA)
Should be Required Prior to Approval of all
Formal International Trade Agreements
Introduction
Scott M. Ferrenberg, Ethan C. Kane, Andrew H.
Smith, and Mark E. Suarez
Department of Entomology, University of Maryland
Throughout history, exchange of goods has
played a major role in shaping societies. Traditionally trade has been considered beneficial for the
involved parties. Not only can trade bolster the
economic situation of nations, it also can diversify
available products and encourage cultural exchanges. As a result, the standard of living is generally increased within the trading nations and the
benefits of trade are often considered to be far
greater than any potential negative consequences.
Seeking these benefits and economic improvements,
many nations lobby for various degrees of free
trade, or for the exchange of goods and commodities in the absence of tariffs, taxes, and embargoes.
There can also be, however, nonbeneficial effects associated with trade. Recently, concerns have
centered on the environmental effects of free trade
and typically have been directed toward the means
of production and differing environmental policies between countries. One consequence environmentalists anticipate is the movement of producers
to those countries with the lowest environmental
standards, where goods can be manufactured at
cheaper rates with minimal focus on reducing pollution. Such considerations are valid; however, the
environmental impacts of trade are not constrained
to industrial pollution and resource use, and the
effects of intentional and unintentional movement
of biota must be included among the concerns.
When introduced either accidentally or intentionally, organisms that are not native to a region
AMERICAN ENTOMOLOGIST • Volume 49 Number 4
out-compete native species for available resources,
reproduce prolifically, and dominate regions and
ecosystems are labeled invasive species. In general,
translocation tends to free species from the ecological pressures imposed upon them by competitors and natural enemies. Left unchecked, invasive
species have the potential to transform entire
ecosystems, as native species and those that
depend on them disappear.
The anthropogenic movement of species is not
a new phenomenon. Whether planned or
unplanned, introductions of species into North
America have been occurring since the preColumbian age. Some species were intended for
release, some escaped from captivity, while others
came as hitchhikers on commodities or as stowaways aboard transport vessels. Although detrimental effects of introductions have been recognized in the past, they were typically dismissed as
an unfortunate side effect of economic progress.
As ecological appreciation and understanding have
burgeoned, many people have come to realize that
these seemingly innocuous introductions may indeed have grave consequences for the health of our
ecosystems and the functions that they perform.
As the desire to curb the introduction of invasive species has grown, so too has the concern that
the trend toward increased free trade holds the
possibility for greater movement of exotic species.
In 1994, Canada, the United States, and Mexico
ratified the North American Free Trade Agreement
(NAFTA), establishing a 15-year timetable to eliminate almost all trade barriers between the three
countries.
The immediate economic gains that trade agreements will garner for participating nations are investigated before ratification. Because it is difficult
to quantify species losses, species reductions, and
habitat destruction into dollar amounts, the economic impacts of environmental degradation have
received little or no attention during formal trade
agreements. So that environmental issues are no
longer ignored, some have proposed that Environmental Impact Assessments (EIAs) be completed
by the United States before any new trade agreements are ratified. An EIA is a systematic examination of the likely effects of development proposals
on the environment before the beginning of any
activity. The actual term is derived from Section
102 (2) of the National Environmental Policy Act
(NEPA) of 1969 (Anonymous 1969). The result
of an EIA is assembled in a document known as an
Environmental Impact Statement (EIS) that
considers the positive and negative effects of a particular project on the environment.
Whether or not EIAs are the best tool for stemming the flow of invasive species into the United
States is the subject of a loquacious and, at times,
acrimonious debate. Given current trends toward
increasingly open trade, and the subsequent risk
of invasive exotic species introduction into the
United States, should an EIA be required before
approval of all formal international trade agreements?
245
Pro Position
Robert C. Venette, Woodward D. Bailey, Daniel A.
Fieselmann, and Juli Gould
U.S. Department of Agriculture, Animal and Plant
Health Inspection Service
More than 50,000 nonindigenous species occur in
the United States (Pimentel et al. 2000). Many of
these organisms were unwittingly brought to the
United States in the course of conducting international trade (Ruesink et al. 1995). The resolution
raises the challenge of simultaneously facilitating
international trade and safeguarding American agriculture and native ecosystems from the establishment of non-indigenous species. This challenge is
part of the mission of USDA’s Animal and Plant
Health Inspection Service (APHIS).
To help fulfill its mission, APHIS uses ecological
risk assessment. Risk assessment evaluates the likelihood of a species becoming established and the
consequences of its establishment. Such assessments
provide a basis for an EIS but are narrower in
scope. This shift in focus remains within the spirit
of the debate and raises two questions: Should we
use risk assessment when conducting international
trade? If so, why?
The international community answers “yes”
to the first question. The Agreement on the Application of Sanitary and Phytosanitary Measures (or SPS agreement) structured under the
World Trade Organization establishes basic rules
for food safety and animal and plant health (FAO
1996). The SPS agreement recognizes that trade
regulations may be necessary to protect human,
animal, or plant health, but prohibits the use of
unsubstantiated claims of risk as a trade barrier.
Risk assessments and resulting regulations must
be based on science (FAO 1996). Formal trade
agreements such as NAFTA include similar SPS
language. Risk assessments generally do not pertain to the development of such large trade agreements, but become pertinent when specific commodities are discussed during bilateral trade negotiations.
At least three reasons account for the broad
support of risk assessment. First, most nations recognize that the best defense against the establishment of exotic pests is preventing them from arriving in the first place. Experience demonstrates that
eradication of an established population can be
exceptionally difficult (Myers et al. 2000). Second,
risk assessments allow countries to target safeguarding efforts. Given the enormous number of
potential invaders, adequate time and resources
do not exist to detect each potential pest as it arrives in a new country. Thus, available resources
are better used if they can be targeted against those
species that pose the greatest risk. Finally, risk assessments may reveal that certain organisms are
not likely to become established in specific parts of
the world (Roberts et al. 1998). As a result, new
trade opportunities may arise that would be economically beneficial. In summary, risk assessments
provide a vital tool to facilitate safe international
246
trade and to protect agriculture and natural resources from risks associated with exotic pests.
Con Position
Gabriella M.G. Zilahi-Balogh, Joan M. Clarke,
Jarrod Leland, and Lois Swoboda
Department of Entomology, Virginia Polytechnical
Institute
Requiring an EIA before Congress could approve
an international trade agreement would be costly
and time-consuming. Congress is already mandated by its constituents to consider issues of public concern such as the environment. Would this
process be improved by instituting an additional
layer of bureaucracy?
Under the National Environmental Policy Act
(NEPA) (Anonymous 1969), only the requirement
of an EIS is enforceable. An EIS is merely a procedural requirement that does not mandate an outcome (Plater et al. 1994). This requirement may
result in distracting environmental groups, but not
in real change that would protect the environment.
This kind of assessment would not be practical for
an entire trade agreement. Specific measures are
needed to reduce introductions of invasive exotic
species. Requiring an EIA would only divert
resources from tasks that could otherwise be used
to reduce the risk of introducing invasive exotic
species into the United States.
Measures are already in place to reduce the risk
of invasive species introductions. The APHIS–Plant
Protection Quarantine (APHIS–PPQ) was delegated
by Congress as the primary Federal agency responsible for preventing the entry and establishment of
invasive plant pests into the United States. Quarantine and inspection requirements provide the
framework for regulation of movement of commodities across United States borders (NPB 1999).
Quarantine pests are identified through a pest risk
analysis process. Economic and environmental concerns are considered in the pest risk analysis procedures (FAO 1996, NPB 1999).
Globalization of trade has influenced international phytosanitary trade requirements. The World
Trade Organization (WTO) and the Food and
Agriculture Organization of the United Nations
(FAO) are the primary sources of international
agreements on plant protection in the context of
international trade. Being a member country, the
United States participates through APHIS–PPQ in
setting international plant health standards and in
trade negotiations with partners worldwide (NPB
1999). Rather than spending resources on EIAs,
directing them toward APHIS would improve the
safeguarding system already in place.
Debate Participants
Clemson University
R. Chitkowski is an M.S. student working with Sam
Turnipseed in cotton.
Michelle G. Colacicco completed her M.S. in December 2000. She examined habitat selection by the red
AMERICAN ENTOMOLOGIST • Winter 2003
imported fire ant under the direction of Peter Adler
and John McCreadie.
Austin Jenkins is an M.S. student working with Sam
Turnipseed and Mike Sullivan in cotton.
Will K. Reeves is a Ph.D. student researching Tabanidae under the direction of Peter H. Adler.
Louisiana State University
Boris A Castro is a Ph.D. candidate examining IPM in
corn and sorghum under the direction of Thomas J.
Riley.
Jeff Gore is a Ph.D. candidate examining IPM in cotton under the direction of Roger Leonard.
Melissa M. Willrich is an M.S. candidate studying integrated pest management (IPM) strategies in soybeans under the direction of David J. Boethel.
North Carolina State University
Fred Gould received his Ph.D. from the State University of New York at Stony Brook in ecology and
evolutionary biology.
University of California at Davis
Kirsten A. Copren is a Ph.D. candidate studying the
behavior, genetics, and taxonomy of termites under
the direction of Rob Page.
David R. Haviland is an M.S. candidate studying integrated pest management strategies in sugarbeets
under the direction of Larry Godfrey.
Cheryle A. O’Donnell is a Ph.D. candidate studying
the systematics of Thysanoptera under the direction of Michael P. Parrella, Peter S. Cranston, and
Penny J. Gullan.
Tamara L. Roush is a Ph.D. candidate examining the
genetic mechanisms of resistance in grapevine, Vitis
sp., to grape phylloxera under the direction of Jeffrey Granett and M. Andrew Walker.
University of Idaho
Patrick S. Duetting is an M.S. student working with
Sanford D. Eigenbrode on tritrophic interactions
among pea aphids, the entomopathogenic fungus
Pandora neoaphidis, and peas.
Mary M. Gardiner is an M.S. student working with
James D. Barbour on the response of the predatory
mites Galendromus occidentalis and Neoseiulus fallacies to Tetranychus urticae.
Addie R. Polerstock is an M.S. student working on the
mating behavior and physiology of Anopheles
gambiae mosquitoes with Marc J. Klowden.
April A. Stehr is an M.S. student working with Joseph
P. McCaffrey on a degree-day model for the cabbage seedpod weevil, Ceutorhynchus assimilis, in
winter canola, Brassica napus.
University of Kentucky
Jerome A. Gels is an M.S. candidate examining horticulture entomology under the direction of Daniel
A. Potter.
David W. Held is a Ph.D. candidate examining horticulture entomology under the direction of Daniel
A. Potter.
Eric J. Marsland is a Ph.D. candidate studying medical-veterinary entomology under the direction of
Stephen L. Dobson.
Marissa L. Griffin is an M.S. candidate examining biological control in field crops under the direction of
Ken V. Yeargan.
University of Maryland
Scott M. Ferrenberg is an M.S. candidate studying popuAMERICAN ENTOMOLOGIST • Volume 49 Number 4
lation and community ecology under the direction
of Robert F. Denno.
Ethan C. Kane is an M.S. candidate studying systematic entomology under the direction of Jeff Shultz.
Andrew H. Smith is an M.S. candidate studying biological control under the direction of Dale Bottrell.
Mark E. Suarez is a Ph.D. candidate examining termite
biology and population genetics under the direction
of Barbara L. Thorne and David J. Hawthorne.
United States Department of Agriculture
Woodward D. Bailey received his Ph.D. from North
Carolina State University specializing in insect physiology and biochemistry.
Daniel A. Fieselmann received his M.S. from the University of Maryland specializing in regulatory entomology and IPM.
Juli R. Gould received her Ph.D. from the University of
Massachusetts specializing in biological control.
Robert C. Venette received his Ph.D. from the University of California-Davis specializing in invasion biology.
Virginia Polytechnical Institute
Joan Marie Clark is an M.S. student in biological control under the direction of Paul Semtner.
Jarrod E. Leland is a Ph.D. student examining biological control with microbes and is under the direction
of Donald E. Mullins.
Lois E. Swoboda is a Ph.D. candidate conducting research in urban/structural pest entomology under
the direction of Dini Miller.
Gabriella Zilahi-Balogh is a Ph.D. candidate conducting biological control research and is advised by
Loke T. Kok and Scott M. Salom.
References Cited
Andrés, L. A. 1985. Interaction of Chrysolina
quadrigemina and Hypericum spp. in California,
pp. 235–239. In E. S. Delfosse [Ed.], Proceedings,
VI International Symposium on Biological Control
of Weeds, 19–25 August 1984, Vancouver, Canada.
Agriculture Canada, Ottawa.
Anonymous. 1969. National Environmental Policy Act
(NEPA) of 1969. Public Law 91-190, 42 U.S. Code
4321-4347, January 1, 1970, 83 Statute 852.
Anonymous. 1984. Biological control act, No. 139.
Northern Territory of Australia, Darwin.
Cairns, J., Jr. 1986. Restoration, reclamation, and regeneration of degraded or destroyed ecosystems,
pp. 465–484. In M. E. Soulé [Ed.], Conservation
biology: the science of scarcity and diversity.
Sinnauer Press, Sunderland, MA.
Caltagirone, L. E., and R. L. Doutt. 1989. The history
of the vedalia beetle importation to California and
its impact on the development of biological control.
Annu. Rev. Entomol. 34: 1–16.
Center, T. D., J. H. Frank, and F. A. Dray, Jr. 1986.
Biological control, pp. 245–263. In D. Simberloff,
D. C. Schmitz, and T. C. Brown [Eds.], Strangers in
paradise: impact and management of nonindigenous
species in Florida. Island Press, Washington, DC.
Crawley, M. J. 1989. The successes and failures of weed
biocontrol using insects. Biocontrol News Info. 10:
213–223.
Davidson, N. A., and N. D. Stone. 1989. Imported fire
ants, pp. 196–217. In D. L. Dahlsten and R. Garcia
[Eds.], Eradication of Exotic Pests. Yale University
Press, New Haven, CT.
DeBach, P. 1974. Biological control by natural enemies.
247
Cambridge University Press, London, U.K.
Delfosse, E. S. [Ed.]. 1988. Proceedings, VII International Symposium on Biological Control of Weeds.
Instituto Sperimentale per la Patologia Vegetale,
Rome.
Dethier, V. G. 1952. Evolution of feeding preferences
in phytophagous insects. Evolution 8: 33–54.
Devine, B. 1999. Clear-cut mission: Communities unite
to free native landscapes from the grip of invasive
species. Nature Conservancy 49: 12–17.
Ehler, L. E. 1991. Planned introductions in biological
control, pp. 21–39. In L. R. Ginzburg [Ed.], Assessing ecological risks of biotechnology. Butterworth
Heinemann, Boston.
Elliott, N., R. Kieckhefer, and W. Kauffman. 1996.
Effects of an invading coccinelled on native
coccinellids in an agricultural landscape. Oecologia
105: 537–544.
Ewel, J. J. 1986. Invisibility: Lessons form south Florida,
pp. 214–231. In H. A. Mooney and J. A. Drake
[Eds.], Ecology of biological invasions of North
America and Hawaii. Springer-Verlag, New York.
FAO (Food and Agriculture Organization of the United
Nations). 1996. International standards for
phytosanitary measures: guidelines for pest risk
analysis. Secretariat of the International Plant Protection Convention, FAO, Rome.
Finkel, E. 1999. Australian biocontrol beats rabbits,
but not rules. Science 285: 1842.
Goeden, R. D., and L. A. Andrés. 1999. Biological
control of weeds in terrestrial and aquatic environments, pp. 871–890. In T. S. Bellows and T. W.
Fisher [Eds.], Handbook of biological control. Academic Press, New York.
SANTE TRAPS
Makers of Malaise traps and other
arthropod collecting devices since 1984.
• Malaise traps
(Townes’style and the
original Malaise
style),
• 2 way Malaise traps
• Canopy traps
• Winkler litter
extractors
• Mini-Winkler litter
extractors
• Litter sifters
• Custom made field
cages of all dimensions
SANTE TRAPS
1118 Slashes Rd.
Lexington, KY 40502
Tel. (859) 268-9534
For more information check out
our website at www.santetraps.com
or contact us at [email protected]
248
Gillman, M., and R. Hails. 1997. An introduction
to ecological modeling. Blackman Hall, Oxford,
UK.
Gurr, G., and S. Wratten. 2000. Biological control:
Measures of success. Kluwer Academic Publishers, Boston.
Hanski, I .A., and D. Simberloff. 1997. The
metapopulation approach, its history, conceptual domain, and application to conservation,
pp. 5–26. In I. A. Hanski and M. E. Gilpin [Eds.],
Metapopulation biology, ecology, genetics, and
evolution. Academic Press, San Diego, CA.
Harley, K. L. S., and R. C. Kassultke. 1971. Tingidae
for biological control of Lantana camara
(Verbenaceae). Entomaphaga 16: 389–410.
Harris, P. 1990. Environmental impacts of introduced biological control agents, pp. 289–300.
In M. Mackauer, L. E. Ehler, and J. Roland
[Eds.], Critical issues in biological control. Intercept Ltd., Andover, UK.
Harris, P. 1993. Effects, constraints, and the future
of weed biocontrol. Agric. Ecosyst. Environ. 46:
289–303.
Hawkins, B. A., and P. C. Marino. 1997. The colonization of native phytophagous insects in North
America by exotic parasitoids. Oecologia
112: 566-571.
Higley, L. G., M. R. Zeiss, W. K. Wintersteen, and
L. P. Pedigo. 1992. National pesticide policy: a
call for action. Am. Entomol. 38: 34–39.
Horsfall, J. G. 1983. Impact of introduced pests
on man, pp. 1–13. In C. L. Wilson and C. L.
Graham [Eds.], Exotic plant pests and North
American agriculture. Academic Press, New
York.
Howarth, F. G. 1983. Classical biocontrol: Panacea
or Pandora’s box. Proc. Hawaiian Entomol. Soc.
24: 239-244.
Howarth, F. G. 1985. Impacts of alien land
arthropods and mollusks on native plants and
animals in Hawai’i, pp. 149–179. In C. P. Stone
and J. M. Scott [Eds.]. Hawai’i’s Terrestrial Ecosystems: Preservation and Management. Proceedings of a symposium held 5–6 June 1984, at
Hawai’i Volcanoes National Park, University of
Hawaii Cooperative National Park Resources
Studies Unit, Honolulu.
Howarth, F. G. 1991. Environmental impacts of
classical biological control. Annu. Rev. Entomol.
36: 485–509.
Howarth, F. G. 2000. Synthesis: The future success
of biological control, pp. 269–403. In G. Gurr
and S. Wratten [Eds.], Nontarget effects of biological control agents in biological control: Measures of success. Kluwer Academic Publishers,
Dordrecht, Netherlands.
Huberty, A. F. 2003. Current issues surrounding the
utilization of genetically modified organisms: A
student debate. Am. Entomol. 49: 38–51.
Husband, B. C., and S. C. H. Barrett. 1996. A
metapopulation perspective in plant population
biology. J. Ecol. 84: 461–469.
Julien, M. H., and R. R. Chan. 1992. Biological
control of alligator weed: unsuccessful attempts
to control terrestrial growth using the flea beetle
Disonycha argentinensis (Col.: Chrysomelidae).
Entomophaga 37: 215–221.
Kahn, E., R. J. Jackson, D. O. Lyman, and J. W.
Stratton. 1990. A crisis of community anxiety
and mistrust: the medfly eradication project in
AMERICAN ENTOMOLOGIST • Winter 2003
Santa Clara County, California, 1981–82. Am. J.
Public Health 80: 1301–1304.
Lofgren, C. S. 1986. History of imported fire ants in
the United States, pp. 36–47. In C. S. Lofgren and
R. K. Vander Meer [Eds.], Fire ants and leafcutting
ants, biology and management. Westview Press,
Boulder, CO.
Louda, S. M., D. Kendall, J. Connor, and D. Simberloff.
1997. Ecological effects of an insect introduced for
the biological control of weeds. Science 277: 1088–
1089.
Mack, R. N., D. Simberloff, W. M. Lonsdale, H. Evans,
M. Clout, and F. A. Bazzaz. 2000. Biotic invasions:
Causes, epidemiology, global consequences, and
control. Ecol. Appl. 10: 689–710.
Malakoff, D. 1999. Fighting fire with fire. Science
285:1841–1843.
McEvoy, P. B. 1996. Host specificity and biological
pest control: How well is research on host specificity addressing the potential risks of biological control? Bioscience 46: 401–405.
McFadyen, R. E. C. 1998. Biological control of weeds.
Annu. Rev. Entomol. 43: 369–393.
McGriff, E., and J. R. Ruberson. 1999. A beltwide
rating of beneficials. Proceedings of the Beltwide
Cotton Conference 2: 1109–1110. National Cotton Council, Memphis, TN.
Myers, J. H., A. Savoie, and E. Von Ramden. 1998.
Eradication and pest management. Annu. Rev.
Entomol. 43: 471–491.
Myers, J. H., D. Simberloff, A. M. Kuris, and J. R.
Carey. 2000. Eradication revisited: Dealing with
exotic species. Trends Ecol. Evol. 15: 316–320.
NPB (National Plant Board). 1999. Safeguarding
American plant resources: A stakeholder review of
the APHIS–PPQ safeguarding system. Conducted
by the National Plant Board (NPB) at the request
of USDA APHIS–PPQ. 133 pp. Downloaded from
http://www.aphis.usda.gov/ppq/safeguarding/
Pimentel, D., L. Lach, R. Zuniga, and D. Morrison.
2000. Environmental and economic costs of nonindigenous species in the United States. Bioscience
50: 53–65.
Plater, Z. J. B., R. H. Abrams, and W. Goldfarb. 1994.
Environmental law and policy: Nature, law and
society. West Publishing, St. Paul, MN.
Randall, J. M., R. R. Lewis III, and D. B. Jensen. 1986.
Ecological restoration, pp. 205–219. In D.
Simberloff, D. C. Schmitz, and T. C. Brown [Eds.],
Strangers in paradise: Impact and management of
nonindigenous species in Florida. Island Press, Washington, DC.
Roberts, R. G., C. N. Hale, T. van der Zwet, C. E.
Miller, and S. C. Redlin. 1998. The potential for
spread of Erwinia amylovora and fire blight via
commercial apple fruit; A critical review and risk
assessment. Crop Prot. 17: 19–28.
Ruesink, J. L., I. M. Parker, M. J. Groom, and P. M.
Kareiva. 1995. Reducing the risk of nonindigenous
species introductions. Bioscience 45: 465–477.
Schardt, J. D. 1986. Maintenance control, pp. 229–
243. In D. Simberloff, D. C. Schmitz, and T. C.
Brown [Eds.], Strangers in paradise: Impact and
management of nonindigenous species in Florida.
Island Press, Washington, DC.
Shafey, O., H. J. Sekereke, Jr, B. J. Houghes, S. Heber,
R. G. Hunter, and R. G. Brooks. 1999. Surveillance
for acute pesticide-related illness during the medfly
eradication program—Florida, 1998. J. Am. Med.
Assoc. 282: 2204–2206.
AMERICAN ENTOMOLOGIST • Volume 49 Number 4
Simberloff, D. 1997. Eradication, pp. 221–228. In D.
Simberloff, D. C. Schmitz, and T. C. Brown [Eds.],
Strangers in paradise: Impact and management of
nonindigenous species in Florida. Island Press, Washington, DC.
Simberloff, D., and P. Stiling. 1997. Risks of species
introduced for biological control. Biol. Conserv. 78:
185–192.
Strong, D. R. 1997. Fear no weevil? Science 277: 1058–
1059.
Thomas, M. B., and A. J. Willis. 1998. Biocontrol—
risky but necessary? Trends Ecol. Evol. 13: 325–
329.
U.S. Congress, OTA (Office of Technology Assessment).
1993. Harmful non-indigenous species in the United
States, OTA-F-565. U.S. Government Printing Office, Washington, DC.
van den Bosch, R., and P. S. Messenger. 1973. Biological Control. Intext Educational Publishers, New
York.
Vinson, S. B. 1997. Invasion of the red imported fire
ant: spread, biology and impact. Am. Entomol. 43:
23–29.
Zwolfer, H., and P. Harris. 1971. Host specificity determination of insects for biological control of weeds.
Annu. Rev. Entomol. 16: 159-178.
Jeffery K. Tomberlin received his Ph.D. from the
University of Georgia specializing in decomposition ecology. He is currently an assistant professor
and extension specialist in the Department of Entomology at Texas A&M University.
PICKUP FROM
Fall 2003
PAGE 178
249